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Population Biology |
2Department of Botany, University of Wisconsin–Madison, 430 Lincoln Drive, Madison, Wisconsin 53706-1381 USA; 3The Great Lakes Indian Fish and Wildlife Commission (GLIFWC), P.O. Box 9, Odanah, Wisconsin 54861 USA; 4Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 20 Nan Xin Chun, Beijing 100093, China
Received for publication June 8, 2004. Accepted for publication February 18, 2005.
ABSTRACT
American wild-rice (Zizania palustris var. palustris) has served as a staple for indigenous North Americans for thousands of years, but has had significant habitat losses in recent centuries. We investigated genetic variability among 17 wild-rice populations in northern Wisconsin using 13 isozyme markers. We then compared these genetic patterns to differences in habitat and population characteristics and phenotypic variation in plant growth and reproduction across sites. Wild-rice's mean genetic diversity (0.15) is moderate compared to wind-pollinated outcrossers but lower than the mean (0.20) reported for the Poaceae. Estimated inbreeding coefficients within populations (f) average 0.12 but vary greatly among the populations (from –0.44–0.52), suggesting heterogeneous population histories. Larger populations in larger lakes express higher levels of genetic variability and smaller inbreeding coefficients than smaller or more isolated populations. The number of panicles per plant is also higher in populations with greater genetic variability. Estimated genetic differentiation among the 17 populations (FST) was high (0.30), suggesting limited gene flow among drainages. Wild-rice population size and degree of isolation have opposing effects on its genetic variability, and plant performance is positively associated with genetic variability.
Key Words: genetic structure • isolation index • life history traits • population size • Zizania
Knowing the manner in which the ecological environment affects population genetic composition and persistence has been a central theme in biological conservation, where much of the connection is constructed through demographic performances of populations. Theoretical results (e.g., Lynch et al., 1995
; Lynch, 1996
) demonstrate that small populations tend to accumulate deleterious mutational load and lose quantitative genetic variation via drift, and population persistence may be threatened as a result. Some of these effects have been observed in natural populations (e.g., Keller and Waller, 2002
). Recent surveys (e.g., Oostermeijer et al., 2003
) stress the importance of building connections between the extent of genetic variation present in populations and population performance. The message is clear that we should obtain and attempt to link ecological, demographic, and genetic variables whenever possible in order to assess the status of a species in its habitats. Although we have accumulated considerable information on the genetic structure of terrestrial plant populations (Hamrick and Godt, 1996a
), similar data for aquatic plants is far less common (Ruckelshaus, 1998
). In fact, aquatic species are in many ways better choices for examining the influence of habitats on populations, as the habitats are easily defined in size.
American wild-rice [Zizania palustris var. palustris (Fassett) Dore] is a native aquatic annual found in wetlands of north-central and eastern North America (Dore, 1969
). It has served as a traditional staple for indigenous peoples for centuries (Johnson, 1969
) as well as a specialty commercial crop more recently (Hayes et al., 1989
). Despite the booming industry related to wild-rice, habitat loss and disruptions of hydrological regimes have caused natural populations of this species to dwindle drastically over the last century (Rogosin, 1951
; Fannucchi et al., 1986
; Meeker, 1993
). The importance of wild rice to native peoples and its ecological role as a food source for wildlife in wetland ecosystems make the conservation of extant natural populations and their genetic variability a serious concern (Waller et al., 2000
).
Environmental conditions, including sediment nutrients (Painchaud and Archibold, 1990
) and plant competition (Lee, 2002
), change the growth of wild-rice. Fluctuating water levels, in particular, may favor the growth of wild-rice by reducing the cover of competing aquatic plants (Thomas and Stewart, 1969
; Meeker, 1993
). Little is known, however, about the manner in which the change of habitats alters population genetic composition and how genetic structure, in turn, affects plant performance, although population size, life history, and reproductive system have been shown to significantly influence patterns of genetic variability (Hamrick and Godt, 1990
; Akimoto et al., 1998
).
Here we report an integrated study of how habitat size and shape, the degree of isolation, and population size affect patterns of genetic variability in American wild-rice in northern Wisconsin. We also compare life history and reproductive characters among populations to see how these reflect (or contribute to) the genetic differences found among populations. By linking genetic components to ecological factors, these results contribute to our ability to improve existing conservation strategies for this important wetland species.
MATERIALS AND METHODS
The species
Earlier work concerning Zizania examined species boundaries (Warwick and Aiken, 1986
; Duvall and Biesboer, 1988
) and the relationship between phenotypic plasticity and genetic variability across species (Counts, 1993
). Two varieties of Z. palustris are recognized: Z. palustris var. palustris (the populations studied here) and Z. palustris var. interior (Dore and McNeill, 1980
; Warwick and Aiken, 1986
; Counts, 1993
) following Fasset's early study on Zizania (1924)
. The two varieties differ in both vegetative and reproductive traits (Warwick and Aiken, 1986
). American wild-rice, Z. palustris var. palustris, is a diploid annual (Kennard et al., 2000
) pollinated mainly by wind. Because the pistillate phase overlaps little with the staminate phase within individual inflorescences (Elliot, 1980
; Goldman, 1990
), outcrossing is considered the major reproductive mode. Natural seed dispersal occurs by water and possibly occasionally via grain-consuming animals.
Field samples and measurements
The 17 wild-rice populations in northern Wisconsin selected for our survey are within one degree of latitude (45°28' to 46°10') but range from 88°59' to 92°32' in longitude (Fig. 1). These populations differ in local population history, size, and water area. Knowing the distribution of the wild-rice populations in Wisconsin, we were able to establish an isolation index to reflect qualitatively the average distance of each sampled population from its nearby populations. The index ranged from 1 (least isolated) to 5 (most isolated; Table 1). We also estimated visually the density of each sampled population using a scale of 1–5, representing sequentially low to high densities. We then estimated overall population size at each site in an arbitrary unit using the product of the relative density and the corresponding population area (Table 1).
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Isozyme study
The leaf samples were immediately frozen in a –80°C freezer upon arrival. Within the following 3 weeks, a 1–2-cm2 piece of each leaf sample was ground in 3–4 drops of cold buffer solution (pH 
6.5) in a conical 1.5-mL tube using a cold (<5°C) mechanical grinder. The buffer solution consisted of 1 mM EDTA, 10 mM KCl, 10 mM MgCl2·6H20, 0.2 M Tris-HCl, 0.1% 2-mercaptoethanol, and 8 g polyvinypolypyrrolidone (PVPP, molecular mass 40 000) per 200 mL of solution. The homogenized leaf samples were placed in the –80°C freezer until use.
We performed horizontal gel electrophoresis on the samples following the procedures of Marty et al. (1984)
. We used three buffer systems in gels of 11.3% starch to assay 12 enzymes. We used buffer number 6 of Soltis et al. (1983)
(Tris/citric acid system, pH 7.8) for glucose-6-phosphate isomerase (GPI; EC 5.3.1.9), aspartate transaminase (ATT; EC 2.6.1.1), alcohol dehydrogenase (ADH; EC 1.1.1.1), esterase (EST; EC 3.1.1.-). We used buffer number 11 (Soltis et al. 1983
; histine/HCl system, pH 7.0) for shikimate 5-dehydrogenase (SKDH; EC 1.1.1.25), malate dehydrogenase (MDH-NAD+ [or MDH1]; EC 1.1.1.40), adenylate kinase (AK; EC 2.7.4.3), and phosphoglucose dehydrogenase (PGDH; EC 1.1.1.44). We used buffer AC of Marty et al. (1983) (histine/citric system, pH 6.5) for alanine transaminase (ANT; EC 2.6.1.2), malate dehydrogenase (MDH-NADP+ [or MDH2]; EC 1.1.1.37), isocitrate dehydrogenase (IDH; EC 1.1.1.42), and phosphoglucomutase (PGM; EC 2.7.5.1).
Estimating the genetic variability, population structure, and gene flow
We used the genotypes scored at these isozyme loci to estimate percentage of polymorphic loci, mean number of alleles at each polymorphic loci, and Nei's gene diversity (Nei, 1972
, 1987
). Because sampled wild-rice populations reside in disjunct habitats, with potentially limited gene exchange, we used Wright's island model (Wright, 1951
, 1965
) to calculate hierarchical F statistics. Assuming neutrality of marker alleles and equilibrium of allelic frequency, this method partitions the overall deficit of heterozygotes among populations (FIT) into an average within-population component due to localized inbreeding (FIS) and an among-population component due to population subdivision and differentiation (FST). The statistics were weighted by population sizes and variances in allele frequencies (Weir and Cockerham, 1984
), jackknifing the results over populations and loci to obtain standard errors. The procedures were carried out using Weir's program DIPLOID.FOR (Weir, 1990
). Using the same island model and by further assuming a linear effect of migration rate on allelic frequency (Wright, 1965
), we also inferred average gene flow among populations. The mean number of successful migrants per generation (= Nm, the population size times the rate of successful migration) was estimated using Wright's formula Nm 
([1/FST] – 1)/4. We also estimated inbreeding coefficients (f) within each population using the average of only polymorphic loci (Weir, 1990
, pp. 54–55).
Statistical tests
We used nonparametric and conservative statistical tests to identify significant associations between genetic parameters of populations and their biotic and physical environments. We compared population inbreeding and genetic diversity between lake and riverine habitats using the Wilcoxon rank sum test (Sokal and Rohlf, 1995
). We also evaluated relationships among ecological factors (lake area, population size, and isolation), the morphological traits, and genetic variables (f and gene diversity) using Kendall's rank correlations. To control for experiment-wise error rate (type I error), we also conducted sequential Bonferroni tests (Rice, 1988
) for comparisons between each measure of genetic variability and ecological parameters (Table 4). No correction was made though for Table 6 because the growth characters are highly correlated and following the Bonferroni correction would substantially inflate type II error.
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). This analysis uses a reference distribution generated by random permutations to test the null hypothesis of independence between the two matrices.
To distinguish between plant size and genetic effects on plant reproductive output, we also applied path analysis (Li, 1975
). Genetic diversity can affect reproductive output both directly and indirectly, via its effect on plant size (Fig. 4). These two effects may be separately estimated from the correlation coefficients observed in the data by the direct path coefficient pd and ps, respectively, and pd,s (the path coefficient from genetic diversity to plant size, estimated to be 0.3 from Table 6). The combined effects of both genetic diversity and plant size can then be estimated in the form of (pd2 + ps2 + 2pdpspd,s).
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Genetic patterns
The 17 populations surveyed inhabited water bodies of various sizes, degrees of isolation, and population densities (Table 1). The 12 isozyme systems yielded 13 interpretable loci, namely: Ant, Mdh2-1, Mdh2-2, Mdh2-3, Pgm, Skdh, Mdh1, Pgdh-1, Pgdh-2, Gpi, Adh, Aat, and Est. Among the 13 loci scored, seven (Skdh, Adh, Gpt, Mdh1, Mdh2, Gpi, and Pgm) were highly polymorphic with at least two alleles in most of the populations (Table 2). In contrast, locus Est had two alleles in four of the 17 populations, and locus Pgdh-2 varied only within the Upper Nine-Mile Lake population. Four loci (Aat, Mdh2-2, Mdh2-3, and Pgdh-1) were monomorphic across all populations. Totogatic Lake had both the largest population area and the highest genetic variability among the 17 populations. The Blaisdell Lake and Spring Lake populations had the lowest levels of genetic variation, but had high levels of observed heterozygosity (Table 2). The most inbred population was the Rice Lake population in Forest County (estimated f = 0.52).
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This study provides the first detailed analysis of genetic variability in Zizania palustris var. palustris and one of the few analyses of any aquatic angiosperm. Among aquatic species, the gene diversity (0.15) of American wild-rice is lower than that of the perennial Carex lasiocarpa (0.27; McClintock and Waterway, 1993
), but similar to that of Asian annual Oryza rufipogon (0.14; Morishima and Barbier, 1990
) and higher than that of South American annual O. glumaepatula (0.003; Buso et al., 1998
). At the species level, the percentage of polymorphic loci (62%) and the population differentiation (FST = 0.30) of American wild-rice resemble corresponding means (62% and 0.28) for the family Poaceae. When compared to the terrestrial system, the mean gene diversity in wild-rice (0.150) is also close to the population average (0.148) reported by Hamrick and Godt (1990)
for wind outcrossers, though significantly lower than the mean reported for the Poaceae (0.20; Hamrick and Godt, 1996a
).
Genetic variability
Both the percentage of polymorphic loci and Nei's gene diversity vary considerably over these 17 wild-rice populations in northern Wisconsin (Table 2). Our analysis suggests that population area/size and degree of isolation are major factors affecting this pattern as their path coefficients are significant and jointly account for 35% and 41% of the variance in genetic diversity and number of polymorphic alleles, respectively.
Genetic variability is positively correlated with population area and to a lesser extent population size (Table 4). Three major processes may initiate this pattern. First, a larger population might receive more migrant pollen, increasing its genetic variation. Second, a larger water body is often associated with a heterogeneous growth environment (Meeker, 1993
). Because additive genetic variance exists for several fitness-related traits in wild-rice (Foster and Rutger, 1980
), selection in different environments could favor different genotypes, allowing genetic variability to increase. Third, the buffering capacity of a large population to catastrophic events is higher than that of a small population, making drift less likely to erode local genetic variability. As these conditions hold for many species, we suspect the positive relationship between population size/ area and genetic variability to be common in aquatic species. Cases showing similar associations have been reported in terrestrial species, such as Salvia pratensis and Scabiosa columbaria (Treuren et al., 1991
), Lychnis viscaria (Lammi et al., 1999
), Ranunculus reptans (Fischer et al., 2000
), and Cochlearia bavarica (Paschke et al., 2002
). Events such as frequent changes in habitat area, human selection, or other perturbations could obscure these relationships, making the associations undetectable in some cases. The populations we surveyed, however, appear relatively stable in these regards.
Wild-rice's genetic variability is affected strongly by the degree of population isolation (Fig. 5) because the highest coefficient of correlation (r = –0.5) was found between population isolation index and percentage of polymorphic loci (Table 4). Although a short population history and a strong selection incurred by human activity or habitat disturbance could both lead to a low genetic variability for a population, our knowledge of the distribution and habitats of the surveyed populations suggests that lack of gene flow may have contributed substantially to the pattern seen here.
Correlations between genetic variability and plant growth and reproduction
These patterns of genetic variation would bear little influence on wild-rice conservation had we not observed the positive associations between the gene diversity of a wild-rice population and certain growth and reproductive traits of the parental generation (Table 6). The traits correlated with gene diversity are fitness-related, including plant size (the maximum stem width and the longest leaf length) and reproductive output (panicle number per plant and the average seed scar number per panicle). Although positive correlations between genetic diversity and fitness within species have been rarely reported (e.g., Lienert et al., 2002
), a combined analysis across multiple species revealed such a positive correlation (Reed and Frankham, 2003
). Higher levels of genetic variability may translate into improved population persistence for wild-rice in natural environments.
Gene flow and population differentiation
Estimated FST is rather high among these wild-rice populations (0.30), suggesting a correspondingly low rate of gene exchange among populations (estimated Nm = 0.59). The migration estimate is necessarily crude due to the assumptions involved in the island model (e.g., Slatkin and Barton, 1989
; Whitlock and McCauley, 1998
). Nevertheless, even a large margin of error still paints a picture of restricted migration among populations. Although wind pollination appears effective in carrying pollen long distances, most pollination still occurs locally. For instance, for the wind-pollinated seagrass Thalassia testudinum, the most effective pollination takes place within 4 km (Schlueter and Guttman, 1998
). Marine eelgrass (Zostera marina) appears similarly geographically structured with FST ranging above 0.20 (Nm 1.1–2.8) and no correlation between geographic and genetic distance (Ruckelshaus, 1998
). Although not strictly comparable, the populations surveyed here span a total of 250 km. Thus, local gene flow among nearby populations must be much higher than between distant populations. As the average gene flow is influenced by the geographic distribution of the populations surveyed, the best comparisons of gene flow among species would include information on the geographical distribution of the populations compared and population sizes.
The estimated low level of gene flow among the 17 populations is consistent with the observed weak correlation between genetic distance and geographic distance by Mantel's test. A similar low correlation has been found in the aquatic species Eichhornia paniculata (Barrett et al., 1993
) and some terrestrial plant (e.g., Schiemann et al., 2000
) and animal species (e.g., Baker et al., 2001
). Conversely, a high level of gene flow among the populations could also homogenize the genetic composition of the populations, diminishing correlations between geographic and genetic distance and leading to a low level of FST as seen in species with continuous distributions in Pinus (Hamrick and Godt, 1996b
).
Inbreeding coefficient and recent population history
Unlike patterns of genetic variability, which frequently reflect the deeper part of a population history, the inbreeding coefficient (f) responds more to recent events. The large variation observed in estimated f (–0.44–0.52) among the wild-rice beds suggests their rather heterogeneous recent histories, including possible changes in outcrossing rate, habitat disturbance, and direct human influence on the populations. The outcrossing rates are yet to be investigated among Z. palustris populations, but large variations in outcrossing rate have been observed in Oryza perennis (Oka and Morishima, 1967
) and O. rufipogon (Morishima and Barbier, 1990
). One source of variation for wild-rice is the percentage of hermaphrodite florets on panicles, which varied from 0.1–0.6 among some Minnesota populations (Liu et al., 1998
). Plant density and duration of anthesis between and among individuals may all bring changes to plant outcrossing rate. As outcrossing rate varies among populations and between years, inbreeding coefficient may fluctuate accordingly.
Wisconsin wild-rice populations differ greatly in their recent histories. Both the Blaisdell Lake and Spring Lake wild-rice populations had low levels of genetic variability, but heterozygosity levels were approximately 40% higher than expected (Table 2), suggesting strong selection. In contrast, the Rice Lake population (Forest County) had relatively high genetic variability and also the highest level of inbreeding among the populations surveyed, suggesting a recent history of population inbreeding, possibly due to some disturbance. The Mud Creek population exhibited high inbreeding and low genetic variability, possibly reflecting a recent population bottleneck.
Implications for wild-rice management
A certain level of genetic diversity is vital to allow populations to respond to short-term shifts in selection and, ultimately, long-term evolutionary challenges (Wilcox and Murphy, 1985
; Hamrick et al., 1991
; Milligan et al., 1994
). If larger populations serve as more effective reservoirs of genetic diversity, protecting water bodies that support such populations represents an important step in managing these populations. However, wild-rice population size or area may fluctuate drastically from year to year (or even through a season), making it important to understand how such processes affect genetic variability and the persistence of unique alleles. Small populations that support high levels of genetic diversity demand special attention, as small populations are often at risk of losing genetic diversity via random genetic drift (Franklin, 1980
; Frankham, 1995
). Isolation index, on the other hand, is another important and knowable factor to consider in conservation plans. Our analysis shows that well-connected populations may preserve more genetic diversity.
Aquatic species rely on specific habitats and dispersal mechanisms, which likely make them subject to different ecological constraints and evolutionary processes than terrestrial plants (Les, 1988
; Barrett et al., 1993
; Laushman, 1993
). In American wild-rice, however, we find levels of genetic variability and population genetic structure similar to those of terrestrial species with similar life histories and breeding systems. Because the growth habit of wild-rice is emergent, a sensible comparison of an aquatic system to terrestrial systems should also include parallel studies on submergent, floating species, as well as on more emergent aquatic species.
FOOTNOTES
1 The authors thank the reviewers for their constructive comments, Kathi Borgmann for lab assistance, Andy Bersch for checking the references, Kandis Elliot for preparing Fig. 1
, the Great Lakes Indian Fish and Wildlife Commission (GLIFWC) for the initial funding and leaf samples, and the Chinese Academy of Sciences for a start-up fund provided to the first author. 
5 Author for correspondence (e-mail: yqlu@ibcas.ac.cn) Present address: Laboratory of Systematics and Evolution, Institute of Botany, Chinese Academy of Sciences, 20 Nan Xin Chun, Beijing 100093, China
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